Competition drives cooperation among closely related sperm of deer mice

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Abstract
Both competition and cooperation between sperm have been well documented, but can individual sperm discriminate between kin, with whom they should cooperate, and non-kin, with whom they should not? Heidi Fisher and Hopi Hoekstra show that when the sperm of two deer mice species are mixed, they aggregate preferentially with sperm from their own species. In mixtures between individuals of the same species, sperm from a monogamous species do not discriminate kin from non-kin, whereas sperm from a promiscuous species do. Sperm can increase their swimming velocity and gain a competitive advantage over sperm from another male by forming cooperative groups, such that selection should favour cooperation of the most closely related sperm. Sperm of deer mice are now shown to aggregate more often with conspecific than heterospecific sperm, in accordance with this theory, whereas in a monogamous species lacking sperm competition, sperm indiscriminately group with unrelated conspecific sperm. Among the extraordinary adaptations driven by sperm competition is the cooperative behaviour of spermatozoa1. By forming cooperative groups, sperm can increase their swimming velocity and thereby gain an advantage in intermale sperm competition1,2. Accordingly, selection should favour cooperation of the most closely related sperm to maximize fitness3. Here we show that sperm of deer mice (genus Peromyscus) form motile aggregations, then we use this system to test predictions of sperm cooperation. We find that sperm aggregate more often with conspecific than heterospecific sperm, suggesting that individual sperm can discriminate on the basis of genetic relatedness. Next, we provide evidence that the cooperative behaviour of closely related sperm is driven by sperm competition. In a monogamous species lacking sperm competition, Peromyscus polionotus, sperm indiscriminately group with unrelated conspecific sperm. In contrast, in the highly promiscuous deer mouse, Peromyscus maniculatus, sperm are significantly more likely to aggregate with those obtained from the same male than with sperm from an unrelated conspecific donor. Even when we test sperm from sibling males, we continue to see preferential aggregations of related sperm in P. maniculatus. These results suggest that sperm from promiscuous deer mice discriminate among relatives and thereby cooperate with the most closely related sperm, an adaptation likely to have been driven by sperm competition.

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